Evolution of threespine stickleback dorsal spines via hoxdb gene regulation

The repeated emergence of similar phenotypes in independent populations is a widespread feature of evolution, yet the extent to which repeated evolution reflects shared molecular mechanisms, and the factors that determine this similarity, remain unclear. Here, we investigate the genetic basis of dorsal spine reduction in threespine stickleback fish, an adaptive trait that has evolved repeatedly in freshwater populations. Phenotypic analyses of crosses between a spine-reduced population from Scotland and the ancestral marine form reveal a major-effect locus, with the spine-reducing allele acting dominantly and influencing body patterning. Bulk segregant analysis maps this effect to a single region on chromosome VI that overlaps the hoxdb gene cluster. Transcriptomic analyses of larval stages show a gain of hoxdb expression in the developing spine region of spine-reduced fish, consistent with the dominance of the derived allele. Together, these results indicate dorsal spine reduction in threespine stickleback through cis-regulatory changes at hoxdb, a mechanism found to mediate dorsal spine evolution in a different species of stickleback fish too. These findings highlight the role of hox genes in adaptive divergence between natural populations within a species and provide a clear example of parallel evolution at the molecular level between species.